The foot and mouth disease (FMD) epidemic in the United Kingdom 2001

The foot and mouth disease (FMD) epidemic

in the United Kingdom 2001

Gareth Davies*

Zinnia, Kettlewell Hill, Woking, Surrey, GU21 4JJ, UK

Abstract

The foot and mouth disease epidemic commenced in February 2001 when diseased pigs were

identified in an abattoir. The infection had become widespread in sheep in England and Wales before

this discovery. It was decided to eradicate the disease by slaughter rather than use vaccine. The virus

was a Pan-Asia O strain that caused few lesions in sheep and this made the identification of infected

flocks very difficult leading to a long drawn-out epidemic. Over four million animals were

slaughtered in 2000 herds and flocks. The last outbreak was in September. q 2002 Published by

Elsevier Science Ltd.

Keywords: Foot and mouth disease; Pan-Asian; Infection

Resume

L’epizootie de fievre aphteuse a commence en fevrier 2001 quand elle a ete identifiee sur des porcs

maladies dans un abattoir. L’infection avait beaucoup diffuse auparavant chez le mouton en

Angleterre et au pays de Galles. Il a ete d’ecide d’eradiquer la maladie par abattage plautot que par

vaccination. Le virus etait une souche Pan-Asia de type O, provoquant des lesions limitees chez le

mouton, ce qui a rendu tres difficile l’identification des troupeaux infectes et conduit a une longue

queue d’epizootie. Plus de quatre millions d’animaux ont ete abattus dand 2000 troupeaux. Le

dernier foyer a ete identifie en Septembre. q 2002 Published by Elsevier Science Ltd.

Mots-cle: Fievre aphteuse; Royaume-Uni; Abattage

1. Introduction

Foot and mouth disease (FMD) was confirmed at an abattoir in Essex, South East

England on February 20, 2001. So began the most disastrous epidemic of this disease to

0147-9571/02/$ - see front matter q 2002 Published by Elsevier Science Ltd.

PII: S0 14 7 -9 57 1 (0 2) 00 0 30 -9

Comparative Immunology, Microbiology

& Infectious Diseases 25 (2002) 331–343

www.elsevier.com/locate/cimid

* Tel.: þ44-1483-772042.

E-mail address: [email protected] (G. Davies).

http://www.elsevier.com/locate/cimid

occur in the country in living memory. It lasted for over 6 months, led to the destruction of

four million animals including 3 million sheep, 600,000 cattle and 138,000 pigs in 2002

infected holdings and 7076 contact premises.

The epidemic cost the national treasury £2.7bn including £1.2bn compensation paid to

farmers for animals slaughtered under control measures, £701m spent on eradication

measures such as the cleaning of infected premises and £471m compensation for animals

killed for welfare reasons. It is estimated that it also resulted in losses in the tourist and

other rural industries amounting to several billion pounds sterling.

2. The beginning of the epidemic

The disease was first recognised in pigs at the Essex abattoir and an 8 km restriction

zone was immediately placed around the premises. The immediate source of the infection

appeared to be a pig fattening unit in Northumberland, near the Scottish border. The unit

fed pigs on swill (waste food) and had sent pigs to the abattoir on February 17.

It is presumed that the swill was contaminated but how the FMD virus entered the UK is

a question still to be answered. As there have been no epidemics of FMD in the European

Union in the recent past the infection must have come from another part of the world.

3. The causative virus

The causative organism was identified as the Pan-Asian strain that belongs to the Near

East-South Asia topotype of type O FMD virus. This strain is particularly virulent and

originated in India in 1990. From there it spread as far west as Greece in 1996 and as far

east as Taiwan province of China in 1997. It has since been identified in Korea, Mongolia,

Russia, Japan and South Africa [1]. Recent outbreaks of FMD in South America have been

due to type A and so these could not be implicated.

4. The initial spread of infection

One characteristic of the Pan-Asia strain is that it produces very few lesions in sheep

and this became of crucial importance in dealing with the epidemic in the UK. It soon

became apparent that the virus had infected sheep in the North of England and that these

had moved through six markets in England, a market in Wales and various dealers

premises before the presence of the disease was recognised and movement controls could

be put in place Fig. 1.

A nationwide ban on the movement of susceptible animals was instituted on February 23.

It was unfortunate that the infection entered the sheep population during the early

spring season when sheep were being transported from winter pastures or were being sold

Fig. 1. Diagram showing connection through markets.

G. Davies / Comp. Immun. Microbiol. Infect. Dis. 25 (2002) 331–343332

G. Davies / Comp. Immun. Microbiol. Infect. Dis. 25 (2002) 331–343 333

for fattening. By February 27, 18 outbreaks had been confirmed and this figure rose to 80

by March 5. Almost all these outbreaks were in sheep and cattle and occurred in the

western and northern upland parts of the country where cattle and sheep rearing is the main

industry.

The first outbreak in Scotland was confirmed on March 1 and on the same day infection

was detected in Northern Ireland. Sheep from a farm in Devon, South West England had

been exported to Germany on February 12 and when the farm was later found to be

infected the exported animals were slaughtered. Further exports were traced through a

dealer to France and to the Netherlands. The French authorities confirmed disease in the

department of Mayenne on March 13 and this was probably due to the importation of

sheep from the UK to a neighbouring unit on February 16. Two outbreaks were reported in

the province of Gelderland and Overijsel in the Netherlands on March 21 and an outbreak

in County Louth, The Republic of Ireland was reported on March 22. The cattle and calves

involved in the Dutch outbreak seemed to have originated from Ireland but had passed

through premises in France.

The early phases of the epidemic were almost entirely in sheep, but within 2 weeks

cases in cattle were being identified. This was a serious development as infected cattle are

capable of producing large quantities of virus that if airborne, could cause further spread of

the infection.

4.1. The shortage of resources

As the epidemic progressed it became clear that there was a serious shortage of

resources. It is essential that FMD infected herds and flocks are detected promptly and

slaughtered as quickly as possible, preferably within 24 h of detection. This time scale was

not being achieved. The consequences of such failure was dramatically illustrated by

graphs produced by epidemiological teams at the Universities of London and Edinburgh

and the Epidemiology Department at the Veterinary Laboratories Agency Weybridge

Fig. 2.

The graph was the outcome of analyses based on mathematical models using data

recorded by the Ministry of Agriculture (MAFF) up to March 19 and it predicted that there

would be a very large epidemic lasting many months. The estimates varied from 70

outbreaks a day to more than 4000 outbreaks by June 2001. One prediction was that, left

unchecked, the epidemic would double in size every 8 days.

The models suggested that more rapid slaughter of infected herds would help to reduce

the spread of infection but that would need to be accompanied by the immediate slaughter

of all susceptible species around infected farms.

This latter policy became known as the ‘contiguous cull’ and the target was to slaughter

infected herds within 24 h and herds in contiguous premises within 48 h. It was also

suggested that, in the worst hit areas, all susceptible animals within 3 km of infected

premises should be slaughtered but this drastic strategy was only implemented in Scotland.

The Ministry of Agriculture was facing difficulties in carrying out these policies. By the

middle of March more than 1200 veterinarians, many from overseas, were employed. Few

had any practical experience of the diagnosis of FMD as even in the UK the last major

epidemic had been in 1967. Additionally the disease was proving difficult to identify in


sheep as the mouth lesions were few and easily confused with Orf, and lesions on the

coronary band were somewhat similar to foot rot and other common conditions.

Major problems were being encountered in the slaughter and disposal of carcases and

the army was called in to assist in the disposal tasks. A disused airfield in Cumbria was

prepared for a mass grave that could contain up to 500,000 carcases and several other sites

for mass graves were identified in other parts of the country. In many places carcases were

burnt but the authorities faced increasing opposition from local inhabitants who

complained at the atmospheric pollution. Rendering facilities were used where possible

but they were insufficient.

While the target of slaughtering infected herds within 24 h and contiguous herds within

48 h was being achieved in some areas this was not happening in Cumbria and there the

strategy was to slaughter out herds and flocks to create a ‘firebreak’ protecting the rest of

the country. In Devon, in the South West of England, there were also a large number of

infected beef and sheep farms but there the policy was to slaughter infected and contiguous

premises and to patrol the remainder. In the event the infection subsided in Devon in June

whereas the last case in Cumbria was in October.

5. Vaccination

There are two alternative strategies in eradicating FMD: slaughter and vaccination.

Vaccination has never been employed in the UK although preparations were made to

distribute vaccine in 1967. In this present epidemic the issue of vaccination arose a number

of times. The first time was during March when the full extent of the epidemic became

Fig. 2. Modellers graph.


clear. The veterinary service made preparations for a vaccination campaign but

Government ministers said they were reluctant to resort to vaccination.

The reasons for this decision, as given by Ministers, were that vaccination did not have

the support of the majority of the farming community, veterinarians, the wider food

industry and even consumers.

The Government had established a committee of scientists to provide scientific advice

(the FMD science group), under the chairmanship of the government’s Chief Scientific

Advisor and they were also reluctant to propose vaccination, partly on the ground that

there was bound to be a delay in immunising the population at risk and partly because they

believed that vaccination would give rise to ‘carriers’ that would cause further outbreaks

and prolong the epidemic. This ‘canard’ was eventually corrected but by that time the

main opportunity to curtail the epidemic by vaccination had been lost.

The number of outbreaks reported each day continued to increase throughout March

and the total reached 1000 by the end of that month. Permission for a limited vaccination

programme in the worst affected areas: Cumbria and Devon had been granted by the

European Commission (Decision 2001/257/EC) and the FMD science group eventually

recommended vaccination of cattle in these areas prior to the animals leaving their winter

quarters, when they might encounter infected sheep. Some 500,000 doses of high potency

vaccine were prepared at the Institute for Animal Health Pirbright and distributed. In the

event this vaccine was not used, largely because of continuing resistance from within the

livestock and food industries.

The farming community was divided on the issue. The larger farmers, particularly

sheep farmers who depended on an export trade, felt that vaccination would cause long

term damage. Many of the smaller farmers and particularly producers of organic meat and

milk products feared that the slaughter strategy would destroy the herds that they had

laboriously created over the last decades and strongly supported vaccination.

6. The peak of the epidemic

The peak of the epidemic came in early April. The number of outbreaks reported each

week fell from 297 in the week commencing on March 26 to 114 in the week commencing

on April 9. The estimated dissemination rate (EDR), providing a measure of the number of

new outbreaks arising from each recorded outbreak, fell from 1.9 in the week commencing

on March 19 to 0.5 in the week commencing on April 9 Fig. 3.

Thereafter there was a steady decline in the number of outbreaks. By the middle of

April infected area restrictions were being lifted in Liecestershire and Northamptonshire

following regular veterinary inspections of all susceptible livestock in the 3 km protection

zone for 21 days followed by sero-surveillance of all sheep and goat flocks within the zone

(each flock sampled so as to identify 5% incidence at a probability of 95%).

Most of the other areas were reporting a reduced number of cases but the disease

appeared to be spreading in South West England, and two further outbreaks were reported

in Northern Ireland on April 14. By April 17 a total of 1,150,000 animals had been

slaughtered and, of these 413,000 carcases still had to be disposed. A further 570,000


Fig

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animals awaited slaughter. Clearly, the available resources were not yet matching the tasks

confronting them.

By the end of April the decline in the epidemic was well established. The number of

cases reported each day was below 10 compared with a peak of 46. However, there were

continuing concerns:

FMD in deer. This concern proved to be unfounded. Numerous samples from deer

showing lesions suggestive of FMD were sent in to the Pirbright laboratory but all

proved to be negative. There has been no evidence of wild deer being implicated in this

epidemic despite the fact that the deer population in Great Britain is now 10 times

greater than in 1967.

Compensation payments for slaughtered stock were reducing the incentive to take

precautions to prevent FMD. This was a continuing concern especially for sheep flocks

whose market value was being eroded by the ban on exports and the closure of markets

and abattoirs.

The failure of some farmers to maintain biosecurity. Advice by the Ministry of

Agriculture was not enforceable by law and lack of compliance appeared to be leading

to continuing spread of disease.

The welfare of livestock confined by movement orders. Movement orders not only

confined stock to the holding but prevented them being moved to outlying pastures in

the same ownership where there was more grass. These orders were slightly relaxed at

the end of April, but nevertheless there were major problems. A livestock welfare

(disposal) scheme was put in place to slaughter stock on holdings where the farmer

could not continue to provide forage for his animals. By the end of the epidemic some

1.3 million sheep, 160,000 cattle and 260,000 pigs had been disposed of under these

arrangements.

7. The tail of the epidemic

The epidemic had largely subsided by the end of April and there were adequate

resources in place to identify and slaughter infected stock. There was hope that the disease

could be eradicated well before autumn when upland sheep were moved to lowland

pastures for the winter but the ‘tail’ of the epidemic proved to be a long one. There were

two main reasons for this.

8. The dispersed structure of many holdings

The first was the pattern of livestock holdings. When the previous major epidemic

occurred in 1967 holdings were relatively small and compact. Since then the average farm

size has increased and to maintain a viable sized unit farmers remaining in the industry

have been buying land sold in the break up of smaller units. These plots of land are often

widely dispersed and there have been cases of up to 15 plots of land, dispersed over several

km, under the same ownership. Animals on these plots are fed by the farmer making


regular visits and in areas where the disease was spreading effective biosecurity was

almost impossible.

9. The infection in sheep

The second reason was that although this epidemic arose from a single source in

Northumberland, by the time it was recognised infected sheep were scattered across the

country. These sheep showed few, if any, clinical signs and often the presence of infection

only became evident when the infected animals came into contact with cattle that became

clinical cases. In effect the 2001 epidemic was a series of mini-epidemics, some of which

gave rise to massive explosions of infection in areas such as Devon and Cumbria where

infected sheep were widespread while others remained hidden as silent infection in sheep

until the summer months when the sheep encountered cattle.

This phenomenon of virtually silent infection in sheep is characteristic of the Pan-Asian

virus, previously unknown in Northern Europe. Epidemics in sheep in countries on the

Mediterranean littoral have died out, apparently of their own accord and probably due to

high ambient temperatures and low humidity preventing the survival of the virus [2]. The

United Kingdom, and particularly the upland sheep raising areas, is cooler and wetter and

it was impossible to forecast whether the epidemic would die out as it had done in Greece.

Slowly epidemiological evidence accumulated that described the cycle of infection in

sheep. Infected animals entering a flock led to the virus spreading within it. The rate of

spread probably depends on the initial challenge, i.e. the number of infected animals

joining the flock and on the contact rate within the flock. Most of the sheep infected in this

epidemic were widely dispersed on moor-lands where the contact rate would be low unless

and until they were gathered together for lambing or shearing.

It appears that the infection cycle of the FMD virus O UK 2001 in individual sheep is

short lived. Experimental infections recorded at the Pirbright laboratory showed that sheep

in contact with sheep experimentally infected with the virus excreted airborne virus

maximally 24 hours after the experimental animals reached peak infectivity. The excretion

of virus by sheep fell into three phases: firstly a highly infectious period of around 7 or 8

days, followed by a period of 1–3 days when trace amounts of viral RNA were recovered

in nasal and rectal swabs. Finally tests on oesophageal- pharyngeal samples 4 weeks after

infection showed that 50% of the sheep carried virus. Antibodies developed around 6–7

days after infection of the contact sheep, coinciding with a sharp decline in viraemia the

in-contact sheep [3]. These laboratory findings indicate that there is a very short incubation

period followed by about a week of infectiousness. Field observations during the epidemic

suggested that the incubation period (time from infection to clinical signs might be some 5

days.

10. Airborne spread

This epidemic was spreading almost entirely in cattle and sheep. While the risk of

airborne virus from pigs is considerable the risk from infected cattle and sheep appears to


be far less. It has been observed [4] that simulations predict that it would require 100 cattle

or sheep to be infected at source for an infectious dose to travel 0.2 km and be sufficient to

infect cattle. In the FMD epidemic in the UK, the level of clinical surveillance is such that

it is unlikely that the number of infected cases in a cattle herd would be as high as 100.

Furthermore the emerging serological evidence suggests that infection has progressed

slowly through sheep flocks during the UK epidemic and so there is a low probability that

100 sheep would be in the early acute phase of infection or clinical disease, simultaneously

[5].

11. Serological diagnosis and surveillance

The diagnostic problems in sheep led to a major programme of serological testing of

sheep in areas surrounding outbreaks. The tests used were:

Tests for virus. Tissue samples were tested initially by the antigen detection ELISA.

Negative Ag ELISA samples were put into tissue culture. Sometimes PCR was performed.

Tests for antibody. Blood samples were tested using a liquid phase blocking ELISA

The apparent eradication of the disease from an area was followed by sero-surveillance:

Blood samples were tested by the solid phase competition ELISA (CELISA). Positive

samples were tested for antibody by the virus neutralisation test.

It has to be borne in mind that no serological test is 100% accurate. Early in the disease

process, virus will be present in blood and tissue samples but later antibody develops and

virus is removed. Applying a test for antibody in the early stages or virus in the later stages

is unlikely to detect an infected animal.

Flocks of sheep in a single ownership may comprise several groups in different fields or

even different holdings. The sampling regime ensured that each group was sampled and a

group was defined as one where the animals within it had touching contact with each other

but no such contact with animals in other groups. After some epidemiological

investigations of known infected flocks where every sheep was sampled it was decided

that groups should be sampled so as to detect 5% incidence with a 95% probability.

Sero-surveillance was carried out in two distinct zones in relation to each infected

premises (IP). Protection zone sero-surveillance was carried out within 3 km radius of

each infected premise and all sheep and goat flocks in that area were sampled. The

sampling was carried out at least 21 days after the cleaning and disinfection of the infected

premises were completed. By the end of October 27 infected flocks had been identified out

of 10,155 flocks sampled.

Surveillance zone (SZ) sero-surveillance was carried out in the area between 3 and

10 km from each IP and the relevant Commission decision (2001/295/EC) demands that

samples are taken from sufficient small ruminant holdings within the zone as is necessary

to detect, at least one infected holding if at least 2% or more flocks were infected (95%

certainty).

By the end of the epidemic 550,000 samples had been tested from 7557 holdings and

evidence of past infection was found in only five flocks. In none of these could virus be

recovered.

It was initially estimated that at least 13,533 flocks would have to be sampled with a


total of 135 million tests. Laboratory facilities were procured at several sites to handle a

volume of 100,000 tests a week.

12. The end of the epidemic

The weeks from the end of April until the middle of September were characterised by a

steady stream of outbreaks. During May, there were some 30 þ outbreaks each week.

These were largely attributable to disease breaking out in the Settle area of Yorkshire, a

cluster of outbreaks in Brecon, Wales, continuing spread in Cumbria and a few scattered

outbreaks in Devon, Durham and elsewhere. The feared increase in outbreaks due to cattle

coming into contact with sheep as they were sent out into the pastures did not materialise.

In June there was some further decline and most of the outbreaks were occurring in

cattle as the infection had reached some areas in Lancashire with dairy herds.

In July local spread in the Thirsk area of Yorkshire threatened districts of Yorkshire and

Humberside that contained large populations of pigs. Again the main feature of the

outbreaks was cattle to cattle transmission. There were some recrudescences in sheep

gathered for shearing showing that there was still the danger of hidden, long standing

infection in sheep flocks.

In August there were further outbreaks in Cumbria and it seemed almost impossible to

eradicate the infection in an area that became known as the ‘Penrith triangle’.

There were further outbreaks amongst sheep on the mountain area of Wales known as

the Brecon Beacons. In some ways this was typical of the whole epidemic: hidden

infection in free-ranging sheep that was only revealed when cattle showed clinical disease.

In late August the disease became confined to Cumbria and Northumberland. The

fragmented structure of the land holdings in these areas favoured cross-infection due to the

movements of farm vehicles. Drastic biosecurity measures were taken and these finally

brought the epidemic to an end. The last outbreak to yield live virus was on a farm in

Allendale, Northumberland on September 24. A further outbreak in that area was

confirmed on positive serological tests on September 29.

These last outbreaks were followed by a follow up programme of mass sero-

surveillance in sheep flocks in the previously infected areas. These revealed little or no

evidence of infection and checks on sero-positive animals failed to reveal virus. The

testing programme continued until the end of November without revealing any further

hidden infection and the last remaining FMD infected area was lifted on November 28.

The epidemic was over.

13. The lessons to be learnt

This epidemic was unique in two ways: it was the first epidemic of FMD in northern

Europe for some 20 years and it was the first epidemic in northern Europe to infect large

numbers of sheep. In many ways it was similar to the Greek epidemic of 1994 in that the

presence of infection was not discovered until had become widespread.

Given that the Pan-Asia strain of virus is likely to be the causative organism of future


FMD epidemics, and given that it produces an almost silent infection in sheep, the

European Union must be prepared for epidemics similar to UK2001 in the near future.

What are lessons to be learnt?

13.1. European livestock are at risk

While the southernmost Member States continue to be at risk from infection in the

Mediterranean basin all states are at risk from infected material coming in from other parts

of the world. Import controls must be improved.

13.2. The structure of the livestock industry risks major epidemics

Recent epidemics of Classical Swine fever have been massive because the pig industry

in various member states has failed to ensure that there are appropriate sanitary barriers to

prevent the spread of infection. Large units in dense livestock populations are supplied

with weaner pigs from distant premises. These are major risk factors. Likewise trading

practices in the sheep industry in Great Britain, in which sheep are moved from market to

market almost invited a major epidemic of disease. The industry must acknowledge these

risks.

13.3. Governments must not neglect veterinary surveillance

Rapidly spreading infectious diseases of livestock can only be identified at an early

stage by constant surveillance on farms, abattoirs and markets. In this epidemic it was only

the observation of lesions in an abattoir that prevented an epidemic that would have

become pan-European.

13.4. Decisions as whether to vaccinate or rely on slaughter must be taken at an early

stage of the epidemic

In the present outbreak a decision to vaccinate was deferred despite clear indications

that the veterinary services did not have sufficient resources to patrol farms and slaughter

and dispose of infected livestock promptly. A decision was taken to slaughter even greater

numbers of animals, the ‘contiguous cull’, which placed even greater burdens on an

overwhelmed service.

13.5. Scientific advice to the authorities must come from one source

In the present epidemic the Government created a ‘scientific group’ to provide advice.

The group had little experience of FMD or of the workings of the livestock industry,

whereas the Veterinary Service had both. Conflicts were bound to occur. If additional

expertise is required in scientific disciplines such as mathematical modelling and

immunology then it should feed into the command that is directly responsible for

executing control measures.


13.6. The public interest must not be neglected

In the past epidemics affected the livestock industry but barely concerned the general

public. This epidemic showed that the public has an interest. It pays for the compensation

and for the control measures, it is affected by the impact on the tourist industry, and it is

increasingly concerned about the welfare of farm animals. Large scale eradication

measures that depend on the expensive, relatively ineffective and highly visible slaughter

of livestock must be a thing of the past.

Acknowledgments

The paper could not have been produced without the assistance of staff at the FMD

epidemology unit, DEFRA. However, the opinions recorded are entirely those of the

author.

References

[1] Kitching RP. A recent history of foot-and-mouth disease. J Comp Pathol 1998;118:89–108.

[2] Mackay D. Epidemiological analysis of the serological survey for antibody to FMD virus,

Greece, unpublished report to FAO; 1994.

[3] Alexandersen, Zhang Z, Reid SM, Hutchins GH, Donaldson AI. Quantities of infectious virus

and viral RNA recovered from sheep and cattle experimentally infected with foot-and-mouth

virus O UK 2001, in press.

[4] Donaldson AI, Alexandersen S, Sorensen JH, Mikkelsen T. Relative risks of the uncontrollable

(airborne) spread of FMD by different species. Vet Record 2001;(148):602–4.

[5] Kitchin RP. Unpublished observations quoted in Ref. [4].


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The foot and mouth disease (FMD) epidemic in the United Kingdom 2001

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